Direct dopamine terminal regulation by local striatal microcircuitry

Nolan, Suzanne O.; Zachry, Jennifer E.; Johnson, Amy; Brady, Lillian J.; Siciliano, Cody A.; Calipari, Erin S.

doi:10.1111/jnc.15034

Cited by 53 publications

(48 citation statements)

References 237 publications

(341 reference statements)

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“…Inhibition of striatal LTSIs via overexpression of Kir2.1, an inwardly rectifying potassium channel, significantly augmented extracellular dopamine evoked by a low dose of amphetamine (Supplemental Figure 1). While this evidence supports an interaction between LTSIs and dopaminergic transmission, multiple potential mechanisms could generate these effects: (1) direct dopamine axon inhibition, (2) disinhibition of local cholinergic interneurons (ChINs), which strongly regulate dopamine 7,11 , and/or (3) disinhibition of local spiny projection neurons (SPNs), which can regulate dopamine via recurrent circuitry 12 .…”

mentioning

confidence: 95%

“…This functional diversity is supported by an array of regulatory mechanisms to control dopamine signals across multiple temporal and spatial regimes. Importantly, local microcircuitry gates dopamine at the terminals, regulating the magnitude, spread, timing, and duration of dopamine signals 7 . A range of local homosynaptic and heterosynaptic mechanisms directly regulate dopamine at striatal terminals 7 , including striatal GABA tone [8][9][10] .…”

mentioning

confidence: 99%

“…Importantly, local microcircuitry gates dopamine at the terminals, regulating the magnitude, spread, timing, and duration of dopamine signals 7 . A range of local homosynaptic and heterosynaptic mechanisms directly regulate dopamine at striatal terminals 7 , including striatal GABA tone [8][9][10] . Given the dynamic activity of LTSIs during reward retrieval, we hypothesized that LTSIs might provide a novel GABAergic mechanism of local dopamine regulation in the striatum with significant implications for learning.…”

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confidence: 99%

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Striatal low-threshold spiking interneurons locally gate dopamine during learning

Holly

Davatolhagh

España

et al. 2020

Preprint

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Low-threshold spiking interneurons (LTSIs) in the dorsomedial striatum are potent modulators of goal-directed learning. Here, we uncover a novel function for LTSIs in locally and directly gating striatal dopamine, using in vitro fast scan cyclic voltammetry as well as in vivo GRAB-DA sensor imaging and pharmacology during operant learning. We demonstrate that LTSIs, acting via GABAB signaling, attenuate dopamine release, thereby serving as local coordinators of striatal plasticity.

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confidence: 95%

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confidence: 99%

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confidence: 99%

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Striatal low-threshold spiking interneurons locally gate dopamine during learning

Holly

Davatolhagh

España

et al. 2020

Preprint

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“…Terminal dopamine release in the striatum does not always correspond with action potentials from ventral tegmental and substantia nigra projection neurons (Trulson, 1985;Mohebi et al, 2019). Release is also regulated by local circuitry, by both homosynaptic and heterosynaptic mechanisms (see Nolan et al, 2020). Functionality of dopamine transporters and release probability (homosynaptic regulation) can both mediate stimulated dopamine release (see Ferris et al, 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Heterosynaptic mechanisms include neurotransmitter release from local interneurons and projection neurons, such as acetylcholine interneurons, which play a major role in regulating local terminal dopamine release (see Cachope and Cheer, 2014;Collins and Saunders, 2020;Nolan et al, 2020). For example, optogenetic stimulation of acetylcholine release drives terminal dopamine release independent of action potential through activation of nicotinic acetylcholine receptors (nAChRs) on dopamine terminals (Threlfell et al, 2012;Cachope et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

A unique multi-synaptic mechanism regulates dopamine release in the nucleus accumbens during adolescence

Pitts

Stowe

Ferris

2020

Preprint

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SummaryAdolescence is characterized by changes in reward-related behaviors, social behaviors, and decision making. These behavioral changes are necessary for the transition into adulthood, but they also increase vulnerability to the development of a range of psychiatric disorders. Major reorganization of the dopamine system during adolescence is thought to underlie, in part, the behavioral changes and increased vulnerability. Here, we utilized fast scan cyclic voltammetry to examine differences in regulation of dopamine release in the nucleus accumbens core of adolescent and adult male rats. We found that differences between adolescent and adult stimulated dopamine release is driven by a unique multisynaptic mechanism in early adolescence involving acetylcholine acting at α6-containing nicotinic acetylcholine receptors to mediate inhibition of dopamine via GABA release. These changes in dopamine regulation across adolescence provides a springboard for our understanding of basic brain development and targeted therapy for a range of psychiatric conditions that emerge in adolescence.

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Evaluation of the potential role of glutamatergic, cholinergic, and nitrergic systems in the dopamine release induced by the pesticide glyphosate in rat striatum

Costas‐Ferreira,

Durán,

Faro

2024

J of Applied Toxicology

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Glyphosate (GLY) is a pesticide that severely alters nigrostriatal dopaminergic neurotransmission, inducing great increases in dopamine release from rat dorsal striatum. This GLY‐induced striatal dopamine overflow occurs through mechanisms not yet fully understood, hence the interest in evaluating the role of other neurotransmitter systems in such effects. So, the main objective of this mechanistic study was to evaluate the possible mediation of the glutamatergic, cholinergic, and nitrergic systems in the GLY‐induced in vivo dopamine release from rat dorsal striatum. The extracellular dopamine levels were measured by cerebral microdialysis and HPLC with electrochemical detection. Intrastriatal administration of GLY (5 mmol/L) significantly increased the dopamine release (1102%). Pretreatment with MK‐801 (50 or 400 μmol/L), a non‐competitive antagonist of NMDA receptors, significantly decreased the effect of GLY (by 70% and 74%, respectively), whereas AP‐5 (400 μmol/L), a competitive antagonist of NMDA receptors, or CNQX (500 μmol/L), an AMPA/kainate receptor antagonist, had no significant effect. Administration of the nitric oxide synthase inhibitors, L‐nitroarginine (L‐NAME, 100 μmol/L) or 7‐nitroindazole (7‐NI, 100 μmol/L), also did not alter the effect of GLY on dopamine release. Finally, pretreatment of the animals with mecamylamine, an antagonist of nicotinic receptors, decreased the effect of GLY on dopamine release by 49%, whereas atropine, a muscarinic antagonist, had no significant effect. These results indicate that GLY‐induced dopamine release largely depends on the activation of NMDA and nicotinic receptors in rat dorsal striatum. Future research is needed to determine the effects of this pesticide at environmentally relevant concentrations.

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Direct dopamine terminal regulation by local striatal microcircuitry

Cited by 53 publications

References 237 publications

Striatal low-threshold spiking interneurons locally gate dopamine during learning

Striatal low-threshold spiking interneurons locally gate dopamine during learning

A unique multi-synaptic mechanism regulates dopamine release in the nucleus accumbens during adolescence

Evaluation of the potential role of glutamatergic, cholinergic, and nitrergic systems in the dopamine release induced by the pesticide glyphosate in rat striatum

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